Imperceptible gamma-band sensory stimulation enhances episodic memory retrieval

Abstract

Enhanced gamma activity (30-100Hz) coincides with the successful recall of episodic memories, but it remains unknown whether this oscillatory activity is a cause or a consequence of the retrieval process. To address this question, we asked human participants to complete a paired associates memory task while undergoing sensory stimulation (at 65Hz, 43.3Hz and 32.5Hz). We observed that 65Hz and 32.5Hz sensory stimulation enhances recall compared to a baseline condition without stimulation. No similar effect was observed following 43.3Hz stimulation. Notably, while almost all participants could perceive 32.5Hz and 43.3Hz sensory stimulation, only a small proportion of participants (∼10%) could perceive the 65Hz visual flicker, suggesting 65Hz sensory stimulation acts as an imperceptible intervention to enhance recall. To understand the dual action of 65Hz and 32.5Hz sensory stimulation on recall, we built three pyramidal-interneuronal network gamma (PING) models and drove them using the same stimulation protocols as in the behavioural task. The behavioural results could be reproduced by stimulating an endogenous ∼32Hz oscillation, but not by stimulating an endogenous ∼65Hz oscillation nor by stimulating a network without an endogenous oscillation. These results suggest that imperceptible 65Hz sensory stimulation enhances recall by harmonically entraining an endogenous ∼32.5Hz oscillation. Based on these findings, we propose that “slow” gamma oscillations play a causal role in episodic memory retrieval.